Anne M. Alvarez
University of Hawaii, Honolulu
Wayne T. Nishijima
University of Hawaii, Beaumont Research Center, Hilo
PostharvestDiseases
of
The papaya (Carica papaya L.), a
native of tropical America, is grown
throughout the tropics and subtropics for
its melonlike fruit, which is usually eaten
fresh. The acropetally produced fruits are
clustered near the top of small (2-8 m),
single-stemmed, herbaceous trees. New
flowers are formed continuously; thus, a
single hermaphroditic tree will have
flowers and fruit in all stages of develop
ment. In Hawaii, the interval from
anthesis to harvest ranges from 22 to 26
weeks. Harvesting begins about 12-15
months after seeding and continues until
the trees become too tall (5-6 m) for
efficient harvesting.
Orchard and postharvest diseases are
very important in reducing yield and
market quality of papaya and are
primarily responsible for the losses that
occur during shipment of the fruit
(3,4,9,11). Postharvest losses of 10-40%
in surface shipments and of 5-30% in air
shipments are not unusual. In a weekly
inspection of 100 hot-water-treated fruit
from five packinghouses during 1986,
24% of 16,985 fruit in simulated air ship
ments were unmarketable (H. M. Couey,
personal communication). Losses due to
diseases ranged from 1 to 93%, depending
on postharvest handling and packing
procedures. The diseases are of three
general types: fruit surface rots, stem-end
rots, and internal fruit infections. The
purpose of this article is to describe and
illustrate the major postharvest diseases
of papaya and to outline the general
methods of disease control.
e 1987 The American Phytopathological Society
PapayaFruit Surface Rots
There are two general types of surface
rots of papaya. The first includes the
diseases caused by fungi that infect
intact, immature, green fruit still
attached to the tree. Anthracnose, choco
late spot, Cercospora black spot, and
Phytophthora fruit rot are examples.
Our discussion does not include Cer
cospora black spot and Phytoph
thora fruit rot because symp
toms usually appear before har-
est and fruits can be culled
before packing (6,19). The
second type of surface rot
ncludes diseases caused by
fungi that infect fruit
through wounds occur
ring before or during
H
« A single isolate of Colletotrichum
gloeosporioides can produce both anthracnose
and chocolate spot, but little is known about
why some lesions remain superficial while
others advance into the fruit parenchyma."
Fig. 1. Common surface rots of papaya fruit: (A) Sunken anthracnose lesion caused by
Colletotrichum gloeosporioides. (B) Cross section of anthracnose lesion showing
grayish white discoloration of papaya flesh. Firm callose tissue forms at the border of the
soft, semicircular lesion. (C) Chocolate spot lesions ranging from minute superficial
spots (left) to large sunken lesions with water-soaked margins (center). (D) Cross section
of chocolate spot lesions showing limited penetration into fruit parenchyma.
(E) Mycosphaerella lesion with light brown, translucent margin. (F) Cross section of
Mycosphaerella lesion showing a layer of firm, black tissue below the infection site.
(G) Soft, translucent Phomopsis lesion with black pycnidia at center. (H) Cross section of
rapidly expanding Phomopsis lesion showing progress of decay into the seed cavity.
harvest. The organisms involved typically
are weak pathogens, such as Myco
sphaerella, Phomopsis, Aliernaria, Stem-
phylium, Fusarium, and Guignardia.
Anthracnose. This disease is caused by
Colletotrichum gloeosporioides (Penz.)
Sacc. Infections usually are initiated in
the field at early stages of fruit
development, but the pathogen remains
quiescent until the fruit reaches the
climacteric phase (13). The fungus may
penetrate the fruit surface directly with
an infection peg (8). An extracellular
cutinolytic enzyme is produced, enabling
the pathogen to enter green, unwounded
fruit. Infection can be inhibited by an
antiserum to cutinase and by several
organophosphorous cutinase inhibitors
(14,15).
When infected fruits begin to ripen,
beads of latex are exuded at the fruit
surface, and small water-soaked spots
appear. As the infection advances, a
circular, sunken lesion with translucent,
light brown margins forms. The fungus
produces light orange or pink spore
masses in the central portion of the lesion
(Fig. 1A). Internal tissue in the infected
area is firm with a grayish white
discoloration that later turns brown (Fig.
IB). A layer of callose forms in the
parenchyma cells, permitting the infected
area to be lifted free of the fruit surface as
a plug (24).
C. gloeosporioides was first considered
to be a wound pathogen of papaya (24),
but direct penetration of the cuticle and
establishment of latent infections were
later demonstrated in laboratory and
field studies (8,13-15). The existence of
latent infections explains why field
sprays often showed delayed effectiveness
in reducing postharvest disease; fruit
lesions were not reduced until 8 weeks or
more after orchard sprays had been
initiated (5,22). The fungicides apparently
protected fruit from new infections but
did not eradicate the subcuticular
quiescent hyphae within the fruit.
Chocolate spot. Minute, superficial
reddish brown lesions are the initial
symptoms of this disease (Fig. IC). As
the fruit ripens, lesions may remain super
ficial (Fig. ID) or enlarge and become
sunken with water-soaked margins.
Anthracnose and chocolate spot have
been described as separate diseases, and
different symptom types were attributed
to different physiological races of C.
gloeosporioides (18). Since this initial
description, M. Aragaki (personal
communication) has determined that a
single fungal isolate can produce both
symptom types, but little is known about
the factors that cause some lesions to
remain superficial while other lesions
advance deeply into the parenchyma of
the fruit.
Dry rot. Dry rot is caused by a
Mycosphaerella sp. that is unable to
penetrate the cuticle enzymatically and
thus is associated with mechanical
682 Plant Disease/Vol. 71 No. 8
injuries. Small wrinkles in the fruit
surface are the first symptoms, and
lesions with brown, translucent margins
develop later (Fig. IE). A layer of hard
tissue may form just below the infection
site, separating the darkened parenchyma
tissue from the epidermal portion of the
papaya fruit (Fig. IF).
The imperfect (pycnidial) stage of
Mycosphaerella sp. was previously
designated Ascochyta caricae Pat.
(18,19), then A. caricae-papayae (Tarr)
(7), but the fungus later was transferred
to Phoma caricae-papayae (Tarr) Punith.
(23). Both ascospores and conidia are
capable of infecting wounded fruit
surfaces (7). In some areas of the tropics,
notably India and Brazil, fruit surface
lesions are common; in Hawaii, the
pathogen usually causes a stem-end rot.
Wet rot. Fruit lesions caused by
Phomopsis sp. occur infrequently but
cause extensive damage (19). The entire
infected area is soft and translucent, and
black pycnidia may form at the central
portion of the lesion (Fig. 1G). A wet rot
proceeds rapidly from the surface into
the fruit cavity (Fig. 1H), and the infected
tissue can be lifted free from the rest of
the fruit. This fungus also is frequently
associated with stem-end rots of papaya.
Alternaria fruit spot. This disease is
characterized by circular to oval black
lesions that become covered with black
spore masses of Alternaria alternata (Fr.)
Keissler (Fig. 2A). Lesions are usually
restricted to the surface of the fruit and
do not cause extensive rotting of the
parenchyma tissues. Refrigeration during
surface shipment enhances disease
development, and symptoms rarely
develop on unrefrigerated fruit.
Alternaria fruit spot previously was a
major disease on fruit grown in papaya
orchards in relatively dry areas of Maui
(5). Alternaria was found to colonize
senescing petioles, and large numbers
(13,700-36,900 spores per fruit) were
found on fruit surfaces at the time of pick
ing; thus, petioles appeared to be the major
inoculum source (I. W. Buddenhagen,
unpublished). Infection was reduced with
biweekly orchard sprays (5) and by post-
harvest hot-water treatments (I. W.
Buddenhagen, unpublished).
Stemphylium fruit spot. Small, round,
dark brown lesions are early symptoms
of Stemphylium infections. Lesions later
enlarge and develop reddish brown to
purple margins (Fig. 2B). Dense, dark-
green spore masses cover the lesions, and
a white to gray mycelium forms at the
lesion center. The pathogen, Stem
phylium lycopersici Yamamoto (= S.
floridanum Hannon & Weber), is
primarily a wound pathogen and usually
occurs on fruit damaged by heat or
refrigeration (10,17).
Fusarium rot. Small dry lesions
develop on the fruit surface and are later
covered by a white, rather compact
myceiial mat (Fig. 2C). The pathogen
Fig. 2. Infrequent surface rots of papaya fruit: (A) Lesions caused by Alternaria alternata
showing black spore masses. (B) Stemphylium lesions characterized by reddish brown
margins and grayish white mycelium. (C) Dry fruit rot caused by Fusarlum solani in which
compact white myceiial mats form overthe lesions. (D) Greenish black lesions associated
with Guignardla sp.
Anne M. Alvarez
Dr. Alvarez, professor of plant pathol
ogy at the University of Hawaii,
received a B.A. degree in biology from
Stanford University and M.S. and Ph.D.
degrees in plant pathology from the
University of California, Berkeley.
Research responsibilities include field
and postharvest studies on etiology
and control of papaya diseases and
bacterial diseases of vegetables and
ornamentals. Current focus is on
serological detection of bacterial
pathogens for epidemiological studies.
Wayne T. Nishijima
Dr. Nishijima, associate extension
plant pathologist at the University of
Hawaii, received a B.S. degree in
forestry from the University of
Washington, an M.S. degree in plant
pathology from the University of
Hawaii, and a Ph.D. degree in plant
pathology from the University of
Wisconsin. His interests and responsi
bilities include plant problem diagnosis,
integrated pest management of
anthurium, field control of postharvest
diseases of papaya, and control of
macadamia diseases.
Plant Disease/August 1987 683
Fig. 3. Stem-end rots caused by various fungi: (A) Stages of stem-end rot caused by
Mycosphaerella sp. showing black, infected tissues with brownish, translucent margins.
(B) Penetration of vascular bundles by Mycosphaerella sp. (C) Successive stages of
infection by Botryodlplodla theobromae. (D) Longitudinal section of stem end showing
bluish black discoloration characteristic of infections by Mycosphaerella sp. and B.
theobromae; fungus has penetrated the vascular bundles. (E) Wrinkled stem-end tissue
characteristic of infection by Phomopsis sp. (F) Phomopsis decay showing soft, light-
brown, translucent parenchyma tissue.
was identified as Fusarium solani sensu
Snyd. & Hans. (19). The disease occurs
sporadically on fruit after harvest.
Guignardia spot. Sunken, greenish
black lesions occasionally observed on
fruit surfaces (Fig. 2D) are associated
with Guignardia sp. (18). Little is known
about this fungus on papaya. This disease
was frequently seen when papayas were
preheated in hot water (42 C) for 40
minutes during postharvest fruit fly
disinfestation, but the incidence subsided
after the preheating time was reduced to
30 minutes.
Stem-end Rots
Stem-end rots of papaya occur when
fungi invade the severed peduncle after
harvest. Spores may also invade through
crevices between the peduncle and the
papaya flesh or invade through small
wounds that occur at harvest. Stem-end
rot initially was attributed only to
Ascochyta sp. (18). Later, other genera,
including Botryodiplodia, Phomopsis,
and occasionally Fusarium (19), were
identified in diseased tissues. We now
know that several other fungi, including
A. alternata, S. lycopersici, C. gloeo-
sporioides, and Mycosphaerella sp.
(5,7,10), also may cause stem-end rots
when inoculated alone or in various
combinations. The most common stem-
end rots are described and compared
here.
Stem-end rot caused by Mycosphaerella
sp. is initially characterized by a
translucent zone around the peduncle. At
early stages, only a slight browning of the
peduncle is apparent as the fungal
hyphae invade the vascular tissue. As the
infection advances, the lesion margin
remains translucent while the remaining
infected tissue becomes black, wrinkled,
and dry (Fig. 3A,B). White mycelium
forms at the stem end at an advanced
stage of infection.
Infections caused by Botryodiplodia
theobromae Pat. have a wide margin of
water-soaked tissue (Fig. 3C) and a
rough surface caused by an irregular
pattern of erumpent pycnidia (19).
Pockets devoid of parenchyma tissue
form in the infected area and later
become filled with mycelium. In longi
tudinal section, the infected vascular
tissue has a bluish black discoloration
resembling infections by Mycosphaerella
(Fig. 3D). In contrast, infections caused
by S. lycopersici are characterized by a
reddish brown discoloration of the
parenchyma tissue, and margins of
diseased and healthy tissue are bright red
to purple.
Tissue infected by Phomopsis sp. first
wrinkles, then becomes translucent and
light green to yellow (Fig. 3E). A band of
water-soaked tissue advances very
rapidly from the infection site toward the
fruit cavity (Fig. 3F), and the infected
portion often can be lifted free from the
684 Plant Disease/Vol. 71 No. 8
rest of the fruit. Pycnidia usually form on
the fruit surface of advanced infections.
Another common and severe post-
harvest disease is caused by Rhizopus
slolonifer (Ehr. ex Fr.) Lind, which at
times is the most destructive of the
postharvest pathogens. The fungus
invades through wounds and rapidly rots
the entire fruit, leaving intact only the
enclosing cuticle. When the fungus
breaches the cuticle, infected fruits
become covered by a mass of coarse gray
mycelium with black macroscopic
sporangia (Fig. 4). In contrast to the
other pathogens, R. stolonifer is capable
of spreading quickly to other fruit in a
container, and an entire carton of fruit
may be rotted within a few days. Never
theless, with careful sanitation and
avoidance of wounds, the disease may be
kept under control.
Internal Fruit Infections
Internal "smut" is a term for fungal
spore masses that fill the fruit cavity. The
disease occurs sporadically when the
blossom end of the fruit is not completely
sealed (Fig. 5). Fungi such as Clado-
sporium sp., Penicillium sp., and
Fusarium spp. may enter through the
narrow passage leading into the seed
cavity and destroy the seed as well as the
surrounding tissue. Infected fruits
usually have a small hole at the blossom
end, often with a light green halo. Fruit
with such symptoms usually ripen
unevenly and are culled before packing
operations. The anatomical disorder
apparently is of genetic origin, and
careful seed selection usually is sufficient
to circumvent this problem. Seed is
collected only from trees in which the
disorder does not occur.
Two bacterial diseases also cause
sporadic damage of papaya fruit.
External symptoms are absent, and the
diseases can be observed only after fruits
are cut open. Purple-stain, caused by
pigment-producing strains of Erwinia
herbicola (Loehnis) Dye (21), is charac
terized by violet to purple streaks in the
vascular tissue and latex ducts surround
ing the seed cavity (Fig. 6A). The
parenchyma tissue becomes translucent
and later rots, producing an offensive
odor and taste.
Internal yellowing disease, caused by
Enterobacter cloacae (Jordan)
Hormaeche & Edwards, is a similar
bacterial disease. The infected fruit flesh
is translucent with a bright yellow to
lime-green discoloration (Fig. 6B). E.
cloacae has been isolated from papaya
fruit, hot-water treatment tanks, papaya
blossoms, and the gut and crop of the
oriental fruit fly (Dacus dorsalis Hendel);
bacterial strains isolated from these
sources reproduced internal yellowing
disease (K. Nishijima, unpublished).
Because of the sporadic occurrence and
lack of external symptoms, modes of
" Because most postharvest diseases
begin in the field, control measures must
also begin in the field; the most effective
approaches are reduction of inoculum
and application of protective fungicides."
Fig. 4. Watery fruit rot caused by Rhizopus
stolonifer. Black masses of sporangia
cover the surface of an infected fruit.
Fig. 5. Internal
Cladosporium sp.
"smut" caused by
Fig. 6. Internal fruit rots caused by
bacteria: (A) In purple-stain fruit rot
caused by pigment-producing strains of
Erwinia herbicola, latex ducts and
vascular tissue surrounding the seed
cavity are discolored. (B) Internal yellow
ing disease caused by Enterobacter
cloacae.
Fig. 7. Effect of hot-water treatment on papayas harvested from the same field and
selected for uniformity. Fruit on the left were treated with hot water for 30 minutes at 48 C
and show no stem-end rot, although ripening is slightly retarded. Fruit on the right were
not treated.
Plant Disease/August 1987 685
infection and spread of these diseases are
poorly understood.
General Measures for Control
of Postharvest Diseases
Measures in the field. Because most
postharvest diseases begin in the field,
control measures must also begin in the
field. Reduction of inoculum and applica
tion of protective fungicides are the most
effective approaches to disease control,
and various chemicals have been tested
for this purpose (16). For papaya, best
control is achieved by frequent sprays of
mancozeb or chlorothalonil, beginning
at first fruit set, about 6-8 months after
planting. The entire fruit and flower
column is sprayed once every 7-14 days
during rainy periods and 14-30 days
during dry conditions. A surfactant is
added to the spray for more efficient
coverage, and a sticker is also used
whenever rainfall of 25 mm per week or
more is anticipated.
Removal of all infected and discarded
fruit is essential for reducing the
inoculum level of postharvest pathogens.
Although removing senescing leaves
from the field is not practical, they should
be removed from the tree on a regular
basis to provide an unobstructed path
between the sprayer and the fruit column
and because such leaves serve as a source
of inoculum in the immediate vicinity of
the fruits.
Infection by fungi that cause stem-end
rot occurs through and around the
severed peduncle sometime after picking
(7). Field sprays substantially reduce the
inoculum level but do not eliminate stem-
end rot infections (5). Adequate control
is achieved only when field sprays are
combined with postharvest hot-water or
fungicide treatments (1,2,11,12).
Resistant varieties. Kapoho Solo, the
major export cultivar, shows no substan
tial resistance to the described postharvest
diseases. It continues to be grown
because it is well adapted to the main
papaya-growing area on the island of
Hawaii and because it has superior horti
cultural and marketing qualities. Sunrise
Solo, the other export cultivar, has some
resistance to infection by C. gloeo-
sporioides (20). Its resistance is sufficient
to preclude spraying for these diseases
except in the wettest areas, but it is highly
susceptible to blight caused by Phytoph-
thora palmivora Butl.
Measures after harvest. Hot-water
immersion or spray followed by applica
tion of fungicides in wax substantially
reduces postharvest decay even for
extended storage during surface shipment
(3,9,11,12). Hot water treatment also
retards ripening (Fig. 7). According to
federal quarantine regulations, papayas
for export to the U.S. mainland must be
less than one-fourth ripe and must be
disinfested for fruit flies within 18 hours
of harvest with a double hot-water
immersion treatment consisting of an
initial 30-minute immersion at 42 C,
followed by a 20-minute immersion at
49 C. The double-dip treatment provides
excellent control of postharvest diseases
of papayas when coupled with regular
field fungicide sprays.
Excessive heating or delayed posttreat-
ment cooling can inhibit the normal
ripening process or scald the fruits,
allowing rapid colonization and serious
postharvest disease problems. Storage
and shipping temperature for papayas
should be at or near 10 C, with as little
fluctuation as possible.
Daily sanitation of the packing line
and the water tanks is necessary to
minimize reinoculation of the hot-water-
treated fruits and particularly to reduce
Rhizopus infections. Equipment and
containers may be disinfested with
quaternary ammonium compounds or
calcium hypochlorite. Chlorine levels in
cold water tanks are maintained at
70-100 ppm at pH 6.0-7.5 to ensure
sufficient chlorine to kill contaminating
organisms.
A number of experimental chemicals
have been tested as postharvest fungicide
treatments to supplement orchard sprays
(1,2,16). Either benomyl or thiabendazole
is effective as a postharvest treatment (2).
The most common postharvest treatment
for surface- and air-shipped papaya is
thiabendazole applied at 4-8 g per
liter with a carnauba wax (3,11,12).
Acknowledgments
We thank the Papaya Administrative
Committee (PAC) and the Governor's
Agricultural Coordinating Committee of the
State of Hawaii for their continuous support
of research on papaya diseases. Results of
PAC-sponsored research appear in the
proceedings of the Hawaii Papaya Industry
Association annual meetings (1976-1986),
published by the University of Hawaii
Cooperative Extension Service, and in
volumes 33, 34, 36, and 38 of Fungicide and
Nematicide Tests.
Literature Cited
1. Alvarez, A. M. 1978. Post-harvest disease
control of papaya with guazatine, Benlate,
and Topsin-M, 1977. Fungic. Nematic.
Tests 33:151.
2. Alvarez, A. M. 1979. Postharvest disease
control of papaya with Benlate, thiabenda
zole, and Dowicide A. Fungic. Nematic.
Tests 34:154.
3. Alvarez, A. M. 1980. Improved market
ability of fresh papaya by shipment in
hypobaric containers. HortScience
15:517-518.
4. Alvarez, A. M. 1980. Doencas fungicasdo
mamoeiro no Havai. Pages 171-178, 187-
196, and 235-243 in: Cultura do Mamoeiro.
Livroceres LTDA, Piracicaba, Brasil.
315 pp.
5. Alvarez, A. M, Hylin, J. W., and Ogata,
J. N. 1977. Postharvest disease of papaya
reduced by biweekly orchard sprays. Plant
Dis. Rep. 61:731-735.
6. Alvarez, A. M., and Nelson, M. G. 1982.
Control of Phytophthora palmivora in
papaya orchards with weekly sprays of
chlorothalonil. Plant Dis. 66:37-39.
7. Chau, K. F., and Alvarez, A. M. 1979.
Role of Mycosphaerella ascospores in
stem-end rot of papaya fruit. Phyto
pathology 69:500-503.
8. Chau, K. F., and Alvarez, A. M. 1983. A
histological study of anthracnose on
Carica papaya. Phytopathology
73:1113-1116.
9. Chau, K. F., and Alvarez, A. M. 1983.
Effects of low-pressure storage on Colleto-
trichum gloeosporioides and postharvest
infection of papaya. HortScience
18:953-955.
10. Chau, K. F., and Alvarez, A. M. 1983.
Postharvest fruit rot of papaya caused by
Stemphylium lycopersici. Plant Dis.
67:1279-1281.
11. Couey, H. M., Alvarez, A. M., and
Nelson, M. G. 1984. Comparison of hot-
water spray and immersion treatments for
control of postharvest decay of papaya.
Plant Dis. 68:436-437.
12. Couey, H. M., and Farias, G. 1979.
Control of postharvest decay of papaya.
HortScience 14:719-721.
13. Dickman, M. B., and Alvarez, A. M.
1983. Latent infection of papaya caused
by Colletotrichum gloeosporioides. Plant
Dis. 67:748-750.
14. Dickman, M. B., Patil, S. S., and
Kolattukudy, P. E. 1982. Purification,
characterization and role in infection of an
extracellular cutinolytic enzyme for
Colletotrichum gloeosporioides Penz. on
Carica papaya L. Physiol. Plant Pathol.
20:333-337.
15. Dickman, M. B., Patil, S. S., and
Kolattukudy, P. E. 1983. Effects of
organophosphorous pesticides on cutinase
activity and infection of papayas by
Colletotrichum gloeosporioides. Phyto
pathology 73:1209-1214.
16. Eckert,J. W., and Ogawa, J. M. 1985. The
chemical control of postharvest diseases:
Subtropical and tropical fruits. Annu.
Rev. Phytopathol. 23:421-454.
17. Glazener, J. A., Couey, H. M., and
Alvarez, A. 1984. Effect of postharvest
treatments on Stemphylium rot of
papaya. Plant Dis. 68:986-988.
18. Hine, R. B., Holtzmann, O. V., and
Raabe, R. D. 1965. Diseases of papaya
(Carica papaya L.) in Hawaii. Hawaii
Agric. Exp. Stn. Bull. 136. 26 pp.
19. Hunter, J. E., and Buddenhagen, I. W.
1972. Incidence, epidemiology and
control of fruit diseases of papaya in
Hawaii. Trop. Agric. (Trinidad) 49:61-72.
20. Nakasone, H. Y., and Aragaki, M. 1982.
Current status of papaya improvement
program. Hawaii Inst. Trop. Agric. Hum.
Resour. Res. Ext. Ser. 033:51-55.
21. Nelson, M. N., and Alvarez, A. M. 1980.
Purple stain of Carica papaya. Plant Dis.
64:93-95.
22. Nishijima, W. T., and Nagata, J. T. 1983.
Field control of postharvest body and
stem-end rots of papaya. (Abstr.)
Phytopathology 73:801.
23. Punithalingam, E. 1980. A combination
in Phoma for Ascochyta caricae-papayae.
Trans. Br. Mycol. Soc. 75:340.
24. Stanghellini, M. E., and Aragaki, M.
1966. Relation of periderm formation and
callose deposition to anthracnose resis
tance in papaya fruit. Phytopathology
56:444-450.
686 Plant Disease/Vol. 71 No. 8